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Keywords:

  • robot-assisted radical prostatectomy;
  • localised prostate cancer;
  • oncological outcomes;
  • urinary continence;
  • erectile function

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

Objective

  • To report combined oncological and functional outcome in a series of patients who underwent robot-assisted radical prostatectomy (RARP) for clinically localised prostate cancer in a single European centre after 5-year minimum follow-up according to survival, continence and potency (SCP) outcomes.

Patients and Methods

  • We extracted from our prostate cancer database all consecutive patients with a minimum follow-up of 5 years after RARP. Biochemical failure was defined as a confirmed PSA concentration of >0.2 ng/mL.
  • All patients alive at the last follow-up were evaluated for functional outcomes using the Expanded Prostate Cancer Index Composite (EPIC) and Sexual Health Inventory for Men (SHIM) questionnaires.
  • Oncological and functional outcomes were reported according to the SCP system. Specifically, patients were classified as using no pad (C0), using one pad for security (C1), and using ≥1 pad (C2) (not including the prior definition).
  • Patients potent (SHIM score of >17) without any aids were classified as P0 category; patients potent (SHIM score of >17) with use of phosphodiesterase type 5 inhibitorsas P1; and patients with erectile dysfunction (SHIM score of <17) as P2 category. Patients who did not undergo a nerve-sparing technique, who were not potent preoperatively, who were not interested in erections, or who did not have sexual partners were classified as Px category.

Results

  • The 3-, 5- and 7-year biochemical recurrence-free survival rates were 96.3%; 89.6% and 88.3%, respectively.
  • At follow-up, 146 (79.8%) were fully continent (C0), 20 (10.9%) still used a safety pad (C1) and 17 (9.3%) were incontinent using ≥1 pad (C2).
  • Excluding Px patients, 52 patients (47.3%) were classified as P0; 41 patients (37.3%) were classified as P1 and 17 patients (15.5%) were P2.
  • In patients preoperatively continent and potent, who received a nerve-sparing technique and did not require any adjuvant therapy, oncological and functional success was attained by 77 (80.2%) patients.
  • In the subgroup of 67 patients not evaluable for potency recovery (Px), oncological and continence outcomes were attained in 46 patients (68.7%).

Conclusions

  • Oncological and functional success was attained in a high percentage of patients who underwent RARP at ≥5 years follow-up.
  • Interestingly, this study confirmed that excellent oncological and functional outcomes can be obtained in the ‘best’ category of patients, i.e. those preoperatively continent and potent and with tumour characteristics suitable for a nerve-sparing technique.

Abbreviations
ADT

androgen-deprivation therapy

BCR

biochemical recurrence

bDFS

biochemical disease-free survival

EPIC

Expanded Prostate Cancer Index Composite

IQR

interquartile range

PDE5

phosphodiesterase type 5

PSM

positive surgical margins

(RA)(R)(L)RP

(robot-assisted) (retropubic) (laparoscopic) radical prostatectomy

SCP

survival, continence and potency

SHIM

Sexual Health Inventory for Men

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

Robot-assisted radical prostatectomy (RARP) is a valuable therapeutic option for clinically localised prostate cancer [1]. The most recent data has shown significant advantages in terms of blood loss and transfusion rates compared with retropubic RP (RRP) [2] and potential advantages for postoperative urinary continence [3] and erectile function recovery [4]. Although the risk of positive surgical margins (PSMs) is at least equivalent between the two approaches, no definitive conclusions can be drawn about biochemical recurrence (BCR), cancer-specific and overall survival because the follow-up duration in existing studies is relatively short and the overall experience with RARP in locally advanced prostate cancer is still limited [5].

Recently, some authors have reported good long-term oncological outcomes after RARP at a median follow-up of 5 years [6] or after a minimum follow-up of 5 years [7, 8]. The 5- and 7-year biochemical disease-free survival (bDFS) rates ranged between 86% and 90%, and 81% and 88%, respectively [6-8]. Although the primary goal of RARP is the complete extirpation of the primary tumour, patients' satisfaction can be negatively affected by the presence of postoperative urinary incontinence and/or erectile dysfunction. Hence, thereis a need to include both oncological and functional outcomes in the assessment of success after RARP. This aspect could be important to better evaluate the quality of the performed surgery. A high percentage of patients with oncological success and functional failure could indicate a surgical technique that compromises the external urinary sphincter, cavernous nerves, or both. Conversely, patients with oncological failure and functional success could be the result of a very conservative surgical procedure with dissection close to the prostate resulting in preservation of the external urinary sphincter and/or cavernous nerves when indeed it was inappropriate to do so. The relevance of these aspects in the methods used to report RARP outcomes were previously highlighted by Ficarra et al. [9]. Unfortunately, previous RARP studies with long-term follow-up did not report the corresponding functional outcomes [6-8]. Recently, Ficarra et al. [9] proposed a novel survival, continence and potency (SCP) system with the aim to appropriately classify all patients who undergo RP according to the oncological and functional outcomesof relevance to them on an individual basis. Specifically, this system's greater generalizability may make it more useful than the currently used ‘trifecta’ and ‘pentafecta’ systems.

The purpose of the present paper was to report the combined oncological and functional outcomes in a series of patients who underwent RARP for clinically localised prostate cancer in a single European centre after ≥5-years follow-up according to SCP outcomes.

Patients and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

We extracted from our Prostate Cancer Database all consecutive patients with a follow-up of ≥5 years after RARP. The collection data was approved by our Institutional Review Board in 2003. Therefore, all clinical and pathological data were prospectively collected. For every patient, the following variables were considered: age, total PSA level, clinical and pathological stage according to the 2002 version of the TNM staging system, biopsy and RARP Gleason score and margin status.

Surgical and pathological examination techniques were previously described in detail [10]. This cohort represents the initial consecutive patients performed by two surgeons using a three-arm da Vinci Surgical System (Intuitive Surgical, Sunnyvale, CA, USA). In 50 patients traditional laparoscopic RP (LRP) was performed by one of the two surgeons before using the robotic assistance. Both surgeons had extensive experience in the field of RRP. All RP specimens were reviewed by two expert uro-pathologists.

After surgery, adjuvant therapies (radiation or androgen-deprivation therapy, ADT) were delivered based on the treating physician's indication. Patients were scheduled to be followed with PSA level determination at 1, 3, 6, and 12 months after RARP; every 6 months for the following 2 years; and annually thereafter. BCR was defined as a confirmed PSA level of >0.2 ng/mL. According to SCP classification, patients treated with adjuvant therapies were classified as Sx category; patients without PSA recurrence as S0 category, and patients with PSA failure as S1 category [9].

All patients alive at the last follow-up were evaluated for functional outcomes. Therefore, all patients who died from prostate cancer or died from other causes were excluded from the analysis. The follow-up was closed in December 2011.

Urinary continence status was assessed using the following item of the Expanded Prostate Cancer Index Composite (EPIC) questionnaire: ‘How many pads or adult diapers per day did you usually use to control leakage during the last 4 weeks?’ [11]. According to SCP classification, patients were classified in three categories: (i) patients not using a pad, C0; (ii) patients using one pad for security, C1; and (iii) patients using >1 pad, C2 (not including the prior definition) [9].

Potency recovery was evaluated using the Sexual Health Inventory for Men (SHIM) questionnaire [12]. Patients potent (SHIM score of >17) without any aids were classified as P0 category; patients potent (SHIM score of >17) with use of phosphodiesterase type 5 (PDE5) inhibitors as P1; and patients with erectile dysfunction (SHIM score of <17) as P2 category [9]. This last subgroup also included patients requiring penile injections, ortransurethral alprostadilfor intercourse. Patients' not evaluable (patients who did not undergo a nerve-sparing technique, who were not potent preoperatively, who were not interested in erections, or who do not have sexual partners) were classified as Px category. Patients receiving a nerve-sparing technique did not receive any penile rehabilitation. However, they are invited to restart their sexual activity using PDE5 inhibitors on demand as soon as possible.

With the aim to summarise in a standardised fashion the combined oncological and functional results in this cohort of patients, we used the squared system proposed by Ficarra et al. [9]. Briefly, an axe system identifies four different squares, including patients with (i) oncological and functional success (square 1), (ii) oncological success and functional failure (square 2), (iii) oncological failure and functional success (square 3), and (iv) oncological and functional failure (square 4).

Parametric continuous variables were reported as the mean (sd), whereas median and interquartile range (IQR) was used for non-parametric continuous variables. Categorical variables were compared using the Pearson's chi-square test. Time from survey to BCR, continence, or potency recovery, were calculated using the Kaplan–Meier method. Patients were censored at the time of BCR (PSA level of >0.2 ng/mL) or at last follow-up if they were BCR-free. Patients were considered continent when stopped using any pads (C0) or continued to use only a safety liner pad (C1). Similarly, patients were considered postoperatively potent when the SHIM score was >17 with (P1) or without the use of PDE5 inhibitors (P0).

All the variables were inserted into a dedicated database and data were analysed by one of the authors using SPSS v.19.0 (IBM Corp., Armonk, NY, USA) software. All reported P values are two-sided and statistical significance was set at P < 0.05.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

From the initial cohort of 198 patients treated between January 2003 and January 2006 in our centre, 15 (7.5%) patients were excluded from the present analysis. Four (2%) patients were lost to follow-up, one (0.5%) patient died from prostate cancer and 10 (5%) died from other causes before the 5-year threshold. Clinical and pathological characteristics of the 183 patients evaluated in the present study are given in Table 1.

Table 1. Clinical and pathological characteristics of 183 patients included in the analysis
VariableValue
Age at diagnosis, years 
Mean (sd)62.3 (6.2)
Median (IQR)63.2 (58–68)
Age at follow-up, years 
Mean (sd)68.5 (6.3)
Median (IQR)69 (64–74)
Baseline total PSA level, ng/mL 
Mean (sd)8.7 (4.9)
Median (IQR)7.5 (5.5–10.3)
Clinical stage, n (%) 
T1c81 (44.3)
T2102 (55.7)
Bioptical Gleason score, n (%) 
≤6134 (73.2)
732 (17.5)
8–1017 (9.3)
D'Amico risk group, n (%) 
Low75 (41)
Intermediate83 (45.4)
High25 (13.7)
Pathological stage (pT), n (%) 
pT2112 (61.2)
pT3a56 (30.6)
pT3b15 (8.2)
Positive surgical margins, n (%) 
Overall29 (15.8)
pT23 (2.7)
pT3a18 (32.1)
pT3b8 (53.3)
Pathological Gleason score, n (%) 
≤6110 (60.1)
751 (27.9)
8–1022 (12)
pN status, n (%) 
pN036 (19.7)
pN12 (1)
pNx145 (79.3)

bDFS

In all, 20 patients (10.9%) were classified as Sx category as they received adjuvant therapies ≤3 months after RARP. Specifically, 16 patients underwent adjuvant radiation therapy and four adjuvant radiotherapy plus ADT. At a mean (sd) follow-up of 81.3 (8.4) months (median 80; IQR 75–86), 143 (78.1%) patients who did not receive adjuvant therapy were classified as S0 (PSA level of <0.2 ng/mL) and 20 (10.9%) as S1 (PSA level of >0.2 ng/mL). In detail, 12 patients with BCR did not receive any additional therapies while eight received external radiation therapy and/or ADT. Figure 1 shows the BCR-free survival in the subgroup of patients who did not receive any adjuvant therapy (S0–1 categories). In detail, the 3-, 5- and 7-year BCR-free survival rates were 96.3%; 89.6% and 88.3%, respectively.

figure

Figure 1. bDFS in patients who underwent RARP without adjuvant therapies (S0–1 categories). The 3-, 5- and 7-year PSA recurrence-free survival rates were 96.3% (163 patients in analysis with six events); 89.6% (163 patients in analysis with 17 events) and 88.3% (141 patients in analysis with 19 events), respectively.

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Functional Outcomes

All patients were preoperatively continent. At follow-up, 146 (79.8%) were fully continent (C0), 20 (10.9%) still used a safety pad (C1) and 17 (9.3%) were incontinent using ≥1 pad (C2). Specifically, continence rates were 39% at 1 month; 73% at 3 months, 87% at 6 months, and 91% at 12 months, respectively. The median (IQR) time to reach continence was 2 (1–3) months (Fig. 2).

figure

Figure 2. Continence recovery in patients who underwent RARP without adjuvant therapies (S0–1 categories). In all, 166 patients attained urinary continence in a median (IQR) of 2 (1–3) months.

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In all, 73 (39.9%) patients were classified as Px category: 39 patients were preoperatively not potent (SHIM score of <17); 32 patients did not have a nerve-sparing procedure for oncological reasons and two patients declared preoperatively to not be interested in sexual activities. Considering the remaining 110 patients, 52 patients (47.3%) were classified as P0 (SHIM score of >17 without any aids); 41 patients (37.3%) were classified as P1 (SHIM score of >17 using PDE5 inhibitors) and 17 patients (15.5%) were P2 (patients with erectile dysfunction). Figure 3 shows the potency recovery rate during the follow-up in the subgroup of patients who underwent a nerve-sparing procedure (excluded Px patients) (Fig. 3). In detail, the 3-, 6-, and 12-month potency recovery rates were 10%, 53% and 82%, respectively. Patients who attained potency needed a median (IQR) time of 6 (6–9) months after RARP.

figure

Figure 3. Potency recovery in patients who underwent nerve-sparing (Px excluded) RARP. Patients P0–1 were considered potent. The median (IQR) time to reach potency was 6 (6–9) months.

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SCP Combined Outcomes

In 20 (10.9%) patient who were treated with adjuvant therapies (Sx), it was possible to evaluate only functional outcomes. In detail, 17 patients (85%) were continent (C0–1) and three (15%) incontinent (C2). Excluding six patients not evaluable for potency outcome (Px), 10 of 14 patients were potent with or without PDE5 inhibitors (P0–1) and four had erectile dysfunction (P2).

In 96 (52.5%) patients preoperatively continent and potent, who received nerve-sparing and did not require any adjuvant therapy, it was possible to combine together the survival (S), continence (C) and sotency (P) outcomes. Conversely, in 67 (36.6%) patients not evaluable for potency recovery (Px) and not receiving adjuvant therapies, it was possible to evaluate only the survival (S) and continence (C) outcomes. Table 2 summarises the different oncological and functional outcomes in these last subcategories.

Table 2. Oncological and functional outcomes in the identified subcategories according to SCP classification
OutcomeAll patients excluded Sx Cx Px patients (96 patients), n (%)All Px patients excluded Sx patients (67 patients), n (%)P
Survival (bDFS):  0.06
Sx  
S088 (91.7)55 (82.1)
S18 (8.3)12 (17.9)
Continence:  0.01
Cx  
C084 (87.5)47 (70.1)
C18 (8.3)10 (14.9)
C24 (4.2)10 (14.9)
Potency:   
Px 
P048 (50)
P135 (36.5)
P213 (13.5)

In the first subgroup of 96 patients, oncological and functional success was reached by 77 (80.2%) patients (square 1). Conversely, 11 patients (11.4%) had oncological success but functional failure (square 2); four (4.1%) had oncological failure but functional success (square 3) and the remaining four (4.1%) failed to reach either oncological or functional outcomes (square 4) (Fig. 4a). In the subgroup of 67 patients not evaluable for potency recovery, oncological and continence outcomes were attained in 46 patients (68.7%) (square 1). While, nine patients (13.5%) had oncological success but were incontinent (square 2); 11 patients (16.4%) were continent but with PSA failure (square 3) and one patient (1.4%) had both oncological and continence failure (square 4) (Fig. 4b).

figure

Figure 4. (a) Schema summarising the results after nerve-sparing RARP in patients who were continent and potent preoperatively (excluding Sx patients). (b) Schema summarising the results in patients not evaluable for potency outcomes (excluded Sx patients).

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

Complete cancer extirpation, postoperative urinary continence, and potency recovery are the most important outcomes in patients who have undergone RP as management of their prostate cancer. Commonly, the main RP outcomes are reported separately, and only a few studies have reported the percentage of patients attaining a combination of these outcomes [9]. The present study is the first to report the combined functional and oncological outcomes after a follow-up of ≥5 years in a cohort of patients who underwent RARP for clinically localised prostate cancer.

After exclusion of patients receiving adjuvant therapies, the 5- and 7-year bDFS rates were 89% and 88%, respectively. These data confirm the results previously reported by Menon et al. [6] and more recently by Sooriakumaran et al. [8] Menon et al. [6] evaluated the long-term oncological outcomes in a series of 1384 consecutive patients with a median (IQR) follow-up of 60 (37.2–69.7) months after RARP. The actuarial bDFS rates were 90.6%, 86.6%, and 81.0% at 3, 5, and 7 years, respectively. Pathological Gleason score 8–10 and pathological stage T3b/T4 resulted the strongest predictors of bDFS in this single-centre study. More recently, Sooriakumaran et al. [8] published the long-term (median [IQR] follow-up of 6.3 [5.6–7.2] years) oncological results of 944 consecutive patients who underwent RARP in a single European institution. The estimated 5, 7, and 9 year bDFS rates were 87.1%, 84.5%, and 82.6%, respectively. A preoperative PSA level of >10 ng/mL, postoperative Gleason sum of ≥4 + 3, pathological T3 disease, positive surgical margin status, and lower surgeon volume, represented the predictors of BCR in this last series. These long-term oncological data can be considered similar to those historically reported after RRP. Therefore, available data also strongly support the oncological safety of RARP in patients with a more consistent follow-up.

Few studies have reported the long-term functional outcomes after RARP [3, 4]. At a median follow-up of 80 months, in the present study the overall continence rate was 91%. Interestingly, continent status was reached in a median time of 2 months and no patients became continent after 12-month follow-up. The present data confirm the published excellent results of continence in RARP. Indeed, considering studies using no pad or a safety pad as the continence definition, 12-month urinary incontinence rates ranged from 8% to 11%, with a mean value of 9%. One paper reported a 36-month urinary incontinence rate of 5%, using the no pad or safety pad definition [3].

Looking at the 96 patients who received a nerve-sparing RARP without adjuvant therapies, the overall potency rate at follow-up was 86.5%. Interestingly, the median time to recovery for erectile function defined by a SHIM score of >17 with or without PDE5 inhibitors was 6 months. No patient became potent 18 months after RARP. Similar to the urinary continence status, potency outcomes also confirmed published data. Indeed, the mean (range) values of reported 3-, 6-, 12-, and 24-month potency recovery rates are 50 (32–68) %, 65 (50–86) %, 70 (54–90) %, and 79 (63–94), respectively [4].

Only a few studies have reported a comprehensive evaluation of RARP outcomes combining functional and oncological outcomes in the so called ‘trifecta’ state. Available data showed that in RARP series the trifecta status characterised by patients without PSA recurrence and postoperatively continent and potent was reached in 53–91% of patients. Clearly, the persistence of postoperative erectile dysfunction is the most important limiting factor to attain the trifecta status [9]. However, the trifecta outcomes only adequately evaluate patients preoperatively continent and potent, undergoing a nerve-sparing technique and not requiring adjuvant therapy postoperatively. Indeed, with the exception of the study published by Xylinas et al. [13] in 2011, the percentage of patients evaluable for the trifecta outcomes was 28–58% of the patients treated in each institution [9]. Moreover, patients failing to reach the trifecta state are a heterogeneous group consisting of patients with oncological success and functional failure, patients with oncological failure and functional success, and patients with both oncological and functional failures. To solve this issue and to improve the methods to report the outcomes after RP, Ficarra et al. [9] proposed the use of the SCP system. The application of the SCP system allowed us in the present series to distinguish between three different categories: (i) patients who received a nerve-sparing technique without adjuvant therapies; (ii) patients who did not receive a nerve-sparing technique or adjuvant therapies; and (iii) patients who received adjuvant therapies after RARP.

The functional outcomes of patients receiving adjuvant radiation therapy, ADT, or both can be negatively affected by these adjuvant treatments, and thus it is not appropriate to assign their outcomes to surgery. Moreover, the bDFS will also be the consequence of combined treatment rather than the results of RP alone. In the present series, 11% of patients were classified in this subgroup. Similarly, inpatients who did not undergo a nerve-sparing procedure, who were not potent preoperatively, or who were not interested in sexual activity during the follow-up (Px), postoperative urinary continence recovery and PSA-recurrence will be the most relevant outcomes. In the present series, 37% of patients were classified in this subgroup. No other study has reported the combination of functional and oncological outcomes in this particular subgroup of patients. Interestingly, the present study showed that only 68.7% of patients attained both oncological and functional outcomes. Oncological outcomes were also attained in an additional 13.5% of patients with urinary incontinence. Looking at the failures, 16.4% had oncological failure and functional success. These data could be the consequence of a less aggressive approach at the level of the prostate apex, especially in patients with tumours located at this level. Excluding patients who were not candidates for a nerve-sparing procedure and those receiving adjuvant therapies, only 52% of the present patients were evaluable for the trifecta outcomes. This percentage is consistent with the value reported by Novara et al. [14] and higher compared with that reported by Patel et al. [15]. In the present study, 80% of patients were continent, potent and with a PSA level of <0.2 ng/mL at the median follow-up of the study (80 months). This percentage is similar to that reported by Shikanov et al. [16] in 2009 and Patel et al. [15] in 2011 and higher than those reported by Novara et al. [14] and Xylinas et al. [13] in 2011. Unlike other published studies, the present data showed that there was oncological failure in only 8.2% of patients. Conversely, the overall risk of functional failure in the same category was 15.5%.

The present study is not devoid of limitations. Firstly, the sample size of this prospective, single-centre study is limited compared with the sample sizes evaluated in other RARP series with long-term follow-up. However, previous studies did not report the long-term functional outcomes but only the estimated bDFS [6, 8]. Moreover, this is the initial series of two robotic surgeons. Therefore, the reported results could be influenced by the learning curve process. Additionally, the surgical technique used during the framework of the present study is different from that more recently used [17]. Theoretically, the use of the fourth-arm da Vinci System, as well as the lateral approach to dissect the bladder neck, the complete athermal antegrade release of the lateral cavernous nerves, the tangential division of the dorsal vascular complex to spare the pubo-urethral ligaments, and the reconstruction of the posterior muscular-fascial plate could further improve the reported results. Moreover, it could be argued that some node-positive patients might have been understaged when omitting pelvic lymph node dissection. In the present series, 59% of patients were classified into intermediate- or high-risk categories. However, only 20% of patients received a standard lymphadenectomy. Finally, we do not have the exact number of PSA determinations for all patients in the present study. However, this limitation is present in most studies investigating BCR after definitive treatment for prostate cancer.

In conclusion, long-term follow-up confirmed that RARP is a valid surgical treatment for clinically localised prostate cancer. Even if potentially influenced by the learning curve process, the present data confirmed that oncological and functional success could be attained in a high percentage of patients who underwent RARP after ≥5 years follow-up. Interestingly, the present study also confirmed that good oncological and functional outcomes can be obtained in the ‘best’ category of patients, i.e. those preoperatively continent and potent and with tumour characteristics suitable for a nerve-sparing technique. The present data should be confirmed by multi-institutional studies with larger sample sizes.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References
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